In their book The Neuropsychology of Anxiety, Jeffrey Gray and Neil McNaughton reframe several important concepts to support their contention that the role of the hippocampus is not just to process spatial information, nor only to contribute to long-term memory consolidation, but rather to perform a more encompassing function of detecting goal conflict. The precise anatomical target of their analysis is actually something they call the septo-hippocampal system, which include all the neuroanatomical structures that receive theta-regulating GABAergic inhibitory signals from the medial septal area. This includes the hippocampus proper, the dentate gyrus, entorhinal cortex, subiculum and the posterior cingulate cortex (Gray & McNaughton, 2002).

Anti-anxiety drugs, both classic and novel, all disrupt theta activity in this system. Furthermore, they are the only class of drug that does so. Lesions to this system produce anti-anxiety effects as well. Gray and McNaughton’s project is thus to build an account of the septo-hippocampal system that accounts for its navigational and mnemonic activities as well as its determining role in the production of anxiety.

Central to their account is the concept of defensive approach. The contrast defensive approach with the defensive avoidance (fight-flight-freeze) system, involving the periaqueductal gray, medial hypothalamus, amygdala and anterior cingulate cortex. This system manages the information, motivation, affect and action plans involved in leaving, escaping or avoiding aversive situations. Defensive approach, on the other hand, involves approaching potentially threatening situations to investigate them. Motivations and affect are mixed, and the animal has to inhibit both the hypothalmically regulated appetitive system and the fight-flight-freeze system in order to enter a risk-assessment mode. Attention must be sharpened, and a level of arousal must be maintained in case an immediate shift into fight-flight-freeze is required.

The septo-hippocampal system can be characterised as a system which accomplishes this behavioural inhibition. It detects and eliminates conflict between "nearly equally primed incompatible goals". Goals encompass both stimuli and response information, can be differentiated by differing response tendencies or differing stimuli to which a response could be made. The system helps eliminate conflicts by increasing the negative valence or weight of affectively negative information. The hippocampus rules things out. This computational strategy is used to explain all of the functions of the hippocampus.

The hippocampus is thus described as a series of comparators, in the tradition of Vinogradova (1975). Gray and McNaughton describe three comparators, a CA3 novelty/familiarity comparator, a CA1 conflict comparator, and a ‘troubleshooting’ comparator in the subiculum, which detects conflict specifically in an animals response tendencies.

A structure of concern pattern emerges from Gray and McNaughton’s account at this point, in their list of circumstances where the troubleshooting function is required; i.e. things that generate conflicting response tendencies. In PAEI order, there are:

P – The Threat of Non-Reward
A – The Threat of Punishment
E – Novelty
I – Relational Processing

P – The Threat of Non-Reward: Potential goal loss or non-reward is still frustrative - a secondary frustrative stimulus (primary would be the actual loss of a reward). The threat of non-reward generates approach-avoidance conflict, and sometimes also fight-flight conflict (or perhaps dominance-submission conflict). These conflicting tendencies have to be inhibited as arousal and attention are increased, to better assess the situation.

A – The Threat of Punishment: This is like the threat of non-reward, but the key emotion is a sense of endangerment which activates the fight-flight-freeze system. Sometimes, however, these urges must be stifled. Animals must venture out under potentially dangerous conditions. Thus they must approach and explore potential dangers (cautiously) to assess the degree of danger involved. The hippocampus inhibits prepotent approach and avoid tendencies while this assessment is being made.

E – Novelty: The hippocampus enables exploration. It receives subcortical input regarding biologically relevant stimuli (potential goals), and compares this with cortical or subcortical mnemonic/motor input. If the comparator receives only subcortical input and no matching cortical information, the potential goal is novel. The hippocampus then determines the strength or weight of the new goal relative to other active or prepotent ones. It inhibits prepotent goals (functioning like an ‘interrupt’ signal), allowing an orientation response, followed by the activation of exploratory behavioral programs.

I – Relational Processing: The isocortex is an associative machine. If it is too promiscuous, many things might be bound together by accident. During information retrieval, too many associations (i.e. information that is not contextually relevant), would be retrieved. The only way the cortex itself could drop inaccurate associations would be to allow those links to weaken over many trials. The hippocampus plays a role in preventing excessive relational binding, and in inhibiting primed associations that are in conflict with the context. This ‘gating’ function has been observed in electrophysiological studies (Grace & Moore, 1988) and modelled computationally (Wagar & Thagard, 2004).

Integrators, in the Adizes formulation, are exquisitely sensitive to social context, and regularly comb through their store of social information, looking for signs of goal conflict, or inconsistencies relevant to the attainment of social goals. Relational processing is a fundamental part (though only a part) of this activity.

Bibliography

1. Gray, J. A., McNaughton, N. (2000) The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-Hippocampal System (2 ed.). (Oxford Psychology Series No. 33). Oxford: Oxford University Press.